Download Ecological Impacts of Alien Species

Overview Articles
Ecological Impacts of Alien Species:
Quantification, Scope, Caveats, and
Recommendations
Despite intensive research during the past decade on the effects of alien species, invasion science still lacks the capacity to accurately predict
the impacts of those species and, therefore, to provide timely advice to managers on where limited resources should be allocated. This capacity
has been limited partly by the context-dependent nature of ecological impacts, research highly skewed toward certain taxa and habitat types,
and the lack of standardized methods for detecting and quantifying impacts. We review different strategies, including specific experimental and
observational approaches, for detecting and quantifying the ecological impacts of alien species. These include a four-way experimental plot design
for comparing impact studies of different organisms. Furthermore, we identify hypothesis-driven parameters that should be measured at invaded
sites to maximize insights into the nature of the impact. We also present strategies for recognizing high-impact species. Our recommendations
provide a foundation for developing systematic quantitative measurements to allow comparisons of impacts across alien species, sites, and time.
Keywords: biological invasions, context dependence, ecosystem functioning, management, prediction
T
he human-mediated translocation of species to regions outside their native ranges is one of the most
distinguishing features of the Anthropocene (e.g., Ricciardi
2007). Although biological invasions are widely recognized
as a key component of current global change, there is much
debate among scientists and other stakeholders concerning, among other things, the scale of the changes caused by
alien species and the extent to which management intervention is warranted (e.g., Richardson and Ricciardi 2013).
This controversy is partly rooted in the lack of a widely
accepted framework for interpreting impacts and a consolidated terminology for impacts to facilitate communication
(Blackburn et al. 2014, Jeschke et al. 2014). One reason for
this lack of consensus may be that such research has involved
only a limited subset of alien species in a restricted number
of regions and environments, which has hindered progress
toward a predictive understanding of impacts in general
(Hulme et al. 2013). There are, however, major gaps in our
knowledge—in particular, how species traits and characteristics of the recipient environments interact to determine the
level of impact (Drenovsky et al. 2012, Ricciardi et al. 2013),
how spatial and temporal scales modulate the interpretation
of impacts (Strayer et al. 2006, Powell et al. 2011), how the
impacts of alien species can be distinguished from other
concurrent and potentially synergistic stressors (e.g., climate
change, landscape alteration; MacDougall and Turkington
2005, Didham et al. 2007), and how different types of
impacts can be evaluated and compared using common metrics and currencies (Parker et al. 1999, Blackburn et al. 2014).
Invasion science needs more-robust methods for reliably
assessing the risks associated with alien species introductions (i.e., the likelihood of their establishment, spread, and
impact), but there is ample research in which this has been
attempted and on why it has been difficult (see, e.g., Leung
et al. 2012, Kumschick and Richardson 2013).
The study of impacts is not a new phenomenon (see e.g.,
Lodge 1993, Mack and D’Antonio 1998). However, only
recently have reviews of the magnitude, scope, and variation
of the impacts of alien species, as well as their geographic and
taxonomic distinctions and biases, substantially expanded
our theoretical knowledge and provided useful conceptual
frameworks (e.g., Vilà et al. 2010, Pyšek et al. 2012, Hulme
et al. 2013, Ricciardi et al. 2013). Further progress hinges on
a more-precise and -comparable quantification of impacts
and on an elucidation of the mechanisms behind them, particularly in the context of local factors (coincident stressors,
BioScience 65: 55–63. © The Author(s) 2014. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
reserved. For Permissions, please e-mail: [email protected].
doi:10.1093/biosci/biu193
Advance Access publication 17 December 2014
http://bioscience.oxfordjournals.org
January 2015 / Vol. 65 No. 1 • BioScience 55
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
SABRINA KUMSCHICK, MIRIJAM GAERTNER, MONTSERRAT VILÀ, FRANZ ESSL, JONATHAN M. JESCHKE, PETR
PYŠEK, ANTHONY RICCIARDI, SVEN BACHER, TIM M. BLACKBURN, JAIMIE T.A. DICK, THOMAS EVANS, PHILIP
E. HULME, INGOLF KÜHN, AGATA MRUGAŁA, JAN PERGL, WOLFGANG RABITSCH, DAVID M. RICHARDSON,
AGNIESZKA SENDEK, AND MARTEN WINTER
Overview Articles
species interactions, and physicochemical conditions that
vary over space and time)—all of which pose challenges
for risk assessment and can misguide management decisions. Here, we assess approaches for quantifying and
prioritizing impacts and provide recommendations for facilitating the risk assessment and management of alien species.
Specifically, we propose guidelines on what information to
collect on the invaded site to better understand the mechanisms of impact and to decide which alien species should
be prioritized for management, on how to plan and conduct
empirical studies to understand impacts, and on how to
approach impact prediction. We follow Ricciardi and colleagues (2013) in defining an impact as a measurable change
in the state of an invaded ecosystem that can be attributed to
the alien species. This definition includes any change in ecological or ecosystem properties but excludes socioeconomic
effects and human values (cf. Jeschke et al. 2014).
Quantifying ecological impacts in the field: What to
measure
Quantitative assessments of alien species impacts are essential to ensure that resources spent on management are prioritized to target the most problematic species, threatened
areas, and affected ecosystem processes (Hulme et al. 2013).
However, in general, the selection of parameters used in
quantitative studies of impact does not seem to have been
sufficiently driven by hypotheses. The selection of appropriate parameters should account for impacts at different
organizational levels, such as individuals, populations, communities, and ecosystem functions (Parker et al. 1999, Pyšek
56 BioScience • January 2015 / Vol. 65 No. 1
The challenge of context dependence
The impacts of alien species vary both in their location and
their duration or frequency, under the influence of local abiotic and biotic variables (Hulme 2006, Ricciardi et al. 2013).
The abundance and performance (e.g., resource uptake,
competitive success) of a species can vary predictably along
physical environmental gradients (Ricciardi 2003, Jokela and
Ricciardi 2008). In addition, the composition of the recipient
community moderates impacts in several ways (e.g., through
resistance or facilitation by resident species; Ricciardi et al.
2013). Interactions between native and alien species may
also vary across physical gradients such that dominance
patterns can even be reversed (Kestrup and Ricciardi 2009).
Finally, other anthropogenic stressors that simultaneously alter the physical and biological environment can
affect many interactions and obscure the effects of alien
species. Figure 1 illustrates this passenger–driver problem of impact attribution, which is a major challenge for
management (MacDougall and Turkington 2005, Didham
et al. 2007); impact attribution could be challenging if the
passenger model dominated. In the driver model, interaction a (or c affecting e) is strong in both directions; in the
passenger model, interaction d (or e affecting b) is strong,
whereas a is weak. Also illustrated are additive (a and e are
strong) and synergistic models (in which a, c, d, and e are
strong).
http://bioscience.oxfordjournals.org
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
Figure 1. The context dependence of alien species impacts.
Knowledge of key interactions and moderating parameters
is required to understand and properly quantify impacts.
The details of these parameters are given in table 1 and
appendix S1.
et al. 2012, Blackburn et al. 2014), and at different levels of
diversity, such as genetic, functional, and taxonomic diversity. Quantifying several impact types at the same site allows
for the determination of causal links among impacts and the
identification of direct and indirect effects (figure 1; see also
Hulme 2006).
Among the most important metrics is alien species abundance, which is correlated with the level of impact, although
not necessarily linearly. The greater the number of individuals or biomass of the alien species is, the more resources
they will use and the greater the extent and strength of
their interactions with native species will be (e.g., Parker
et al. 1999, Ricciardi 2003). Catford and colleagues (2012)
provided a practical way of taking the abundance of alien
species into account: identifying abundance thresholds and
using ­categorical scores.
Time since invasion also influences the level of impact,
through temporal changes in the abundance of the alien
species, adaptation by the recipient community, postinvasion
evolution, and variation in the physicochemical environment in the invaded range (Strayer et al. 2006, Dostál et al.
2013). The introduction or establishment date should therefore be noted. The magnitude, direction and type of impact
also vary with the spatial extent and grain (resolution) of
the study area (e.g., Gaertner et al. 2009). It is therefore
important to indicate sampling plot size as well as the area
over which plots were sampled, also in light of species–area
curves. However, this measure might not always be straightforward—for example in the case of migrating animals.
Overview Articles
The prioritization of management
It is beyond the scope of this study to discuss management
prioritization if the passenger model dominates for a particular system. In the following section, we therefore only
address impacts in situations in which the alien species is
most likely to be a driver of the impact.
For efficient and cost-effective allocation of management
resources, there is a strong need to flag those alien species
with potentially high environmental impacts (Blackburn et
al. 2014). It has been proposed that species with the potential
to force ecosystems to cross biotic and abiotic thresholds—
and, therefore, to change to alternative states (i.e., causing
regime shifts)—should be considered as potentially the
most disruptive and should be given top priority for intervention (Gaertner et al. 2014). Regime shifts are associated
with a reorganization of the internal feedback mechanisms
that structure an ecosystem, such as plant–soil feedbacks
(Scheffer et al. 2012). However, at present, it is difficult to
predict whether a given species can alter feedbacks in ways
that could lead to a regime shift. The outcomes depend
on the traits of the alien species, the characteristics of the
invaded habitat and of the invaded community (figure 1;
Pyšek et al. 2012, Kueffer et al. 2013), and interactions
between these factors (Ricciardi et al. 2013). One way of
tackling these challenges is to identify specific combinations
of species traits, ecosystem characteristics, and impacts with
a high probability of causing changes in ecosystem feedbacks
(Gaertner et al. 2014). Such feedbacks are commonly associated with the impacts of ecosystem engineers (table 1 and
supplemental appendix S1; Linder et al. 2012, Ricciardi et al.
2013).
If no quantitative or statistically comparable data are
available, as is often the case, impact-scoring systems can be
used to make very diverse data comparable. Furthermore,
they allow comparisons between groups with different
impact mechanisms (Kumschick et al. 2012, Blackburn et al.
2014). Scoring systems have been used to identify traits
of alien mammals and birds associated with high levels of
impact (Nentwig et al. 2010, Kumschick et al. 2013) and have
shown that the diversity of habitats that an alien species can
occupy could be a useful parameter in models predicting
that species’ impact (Evans et al. 2014).
http://bioscience.oxfordjournals.org
Implications for prediction and prevention
We need to mitigate impacts not only when aliens are
present but, ideally, also when they are expected to invade
and likely to have an undesirable impact in the future.
Preinvasion assessments with the purpose of predicting
the risk of invasion and impact are used in many parts
of the world (Kumschick and Richardson 2013), but the
impact assessment is generally not convincingly incorporated, owing mainly to the same inherent difficulties
and uncertainties that account for the lack of a robust
predictive framework and a lack of data on impacts in
general. A potential solution would be to identify predictable patterns via statistical synthesis of data from multiple
sites for given species—ideally, those with a sufficiently
documented impact history (figure 2; Kulhanek et al.
2011). Such studies can also contribute to the justification
for labeling a species as a potential invasive or as causing
a potential impact elsewhere as an often-suggested predictor of invasion success and impact, respectively, in the
new range (Leung et al. 2012, Kumschick and Richardson
2013). Figure 2 outlines a logical series of empirical
approaches for forecasting impacts, primarily on the basis
of impact and invasion history. Vitousek (1990) posited
that alien species that have large effects on ecosystem
processes differ from the native species in their resource
acquisition, resource efficiency, or capacity to alter disturbance regimes; examples of this include alien plants that
change fire regimes following their introduction, such
as many invasive grasses (D’Antonio and Vitousek 1992,
Yelenik and D’Antonio 2013), and mammalian predators
introduced to islands with no evolutionary history of
such species or archetypes (e.g., Blackburn et al. 2004).
The functional distinctiveness of the alien species may
enhance its impact through novel resource use and exposure to ecologically naive residents or by introducing new
ecosystem functions (e.g., nitrogen fixers in communities
naturally without such a guild). Taxonomic or phylogenetic distinctiveness can serve as proxy parameters of
functional distinctiveness (Ricciardi and Atkinson 2004,
Strauss et al. 2006). In some cases, however, alien species
may differ not in functional type but in performance and
behavior. For example, alien and native predators may differ in their feeding behaviors toward a common prey, but
these differences can be quantified and compared by testing their functional response (Dick et al. 2014).
Finally, one aspect of potentially high predictive value that
has not been adequately explored is whether the impacts of
alien species are similar to those of phylogenetically closely
related or functionally similar alien species. This relationship
is often assumed and used to assess the risk of species that
have not been introduced elsewhere (e.g., Bomford 2008),
but it has rarely been tested. A cursory examination of the
freshwater literature indicates that taxonomic affiliation—
whether a species is closely related to a proven invader—is
not a consistent predictor of impact potential (Ricciardi
2003).
January 2015 / Vol. 65 No. 1 • BioScience 57
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
An increased understanding of context dependence is
required in order to improve our ability to predict impacts.
Resource managers can play a valuable role in their initial
detection and by providing information on the shifting contexts of impacts, through their observation of environmental
change. However, quantifying these changes requires considerable research and sufficient resources. Governments, landowners, and managers, as well as the general public, could
profit from the outcomes of such studies. Moreover, funding should be allocated by all of these stakeholders to both
research institutes and land management agencies. The outcomes can then feed into preventive measures—for example,
to improve risk assessments and management plans.
Overview Articles
Table 1. Suggested parameters important for quantifying, predicting, and prioritizing the management of the impact
of alien species.
Parameter
Rationale
Quantification
Changes to ecosystem function following
invasion
Changes to ecosystem functions often affect ecosystem services.
Per capita effects
The level of impact is a function of per capita effects (e.g., the rate of
resource uptake), abundance, and interactions between organisms and their
environment.
Composition and abundance of native
species and traits in the recipient community
Recipient communities can be transformed rapidly by interacting with alien
species. Native species may increase or decrease in abundance (or even
become extirpated). Food webs may be altered because of the addition or
deletion of energy pathways.
Genetic composition of congeneric native
species in the recipient community
Introgression may affect native gene pools.
Abiotic changes following invasion
Altered physicochemical processes affect species interactions and
ecosystem functions.
Spatial scale
The overall spatial extent of impact depends on species distribution.
Time since introduction
Impact varies over time, owing to changes to local abiotic conditions, the
abundance of the invader, and the response of the recipient community.
Other stressors during invasion
Identification of simultaneous biological (e.g., other invaders) and
environmental stressors (e.g., climate change, nutrient pollution, land
transformations) can have multiple additive or synergistic effects. It is
necessary to disentangle these confounding effects to resolve whether the
invasion is the cause or the symptom of any impact.
Impact history of the invader
The impact history of a species, if well documented, is the most reliable
predictor of its impact, although context-dependent influences can cause
unexpected outcomes.
Abundance of the invader
In many cases, the level of impact scales with abundance (at least initially).
Elucidation of the relationship between abundance and impact will assist
in developing species-specific predictive models and for determining
thresholds for regime shifts.
Functional or phylogenetic novelty
(distinctiveness) of the invader respective to
native community
Larger impacts are often caused by alien species that are functionally or
phylogenetically distinct from the recipient community.
Endemism
Native species that have been geographically isolated over evolutionary time
scales are naive to the effects of a broad range of alien species.
Ecosystem services
Identification of the affected ecosystem services can guide management
prioritization and facilitate communication with various stakeholders.
Rare and Red-listed species
Red-listed species are of priority conservation concern and should be
protected against the threat of alien species.
Conservation concern of the invaded
ecosystem
Prioritization of alien species management depends on the nature of the
ecosystem invaded (e.g., protected area, sanctuary).
Native biodiversity
Diverse native assemblages are deemed to have more conservation value.
Ecosystem engineers
Feedbacks, potentially leading to regime shifts, are commonly associated
with the impacts of ecosystem engineers.
Context
dependence
Prediction
Management
prioritization
Note: The listed parameters do not cover every potential type of ecological impact (e.g., literature reviews of plant invasions have identified at
least 15 broad types of impact that are repeatedly measured; see Pyšek et al. 2012, Hulme et al. 2013). Rather, the selection is driven by
considerations for the provision of guidance for improving the consistency and comparability of the impacts of invasive species among studies
(e.g., meta-analysis) and to elucidate context dependency, therefore increasing insights into species- and site-related variation and possibilities
for predictions based on impacts previously recorded elsewhere. More detailed information on specific parameters and references appear in
appendix S1.
Understanding the mechanisms behind an impact is
ultimately important to predicting the impacts of new alien
species with no alien relatives. Trait-based models can give
indications of such mechanisms, but, so far, it has not been
explored to what degree traits correlated with impact have a
predictive value for new invaders (Evans et al. 2014).
Experimental methods and approaches to
investigate impacts
Various approaches have been taken to study the impacts
of different taxa in different habitat types (supplemental
58 BioScience • January 2015 / Vol. 65 No. 1
appendix S2). Most of these studies have involved comparisons of invaded and uninvaded reference sites, primarily at
the fine resolution of plots and their restricted extent (a
in figure 3). This approach is commonly used to infer the
impacts of alien species on particular native species, on community structure (i.e., species diversity), and on ecosystem
processes such as nutrient pools and fluxes (Vilà et al. 2011).
If suitable reference plots are available, it is the simplest
observational approach, because it allows large amounts
of data to be collected relatively easily and inexpensively.
However, it does not demonstrate causality, because the
http://bioscience.oxfordjournals.org
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
Purpose
Overview Articles
http://bioscience.oxfordjournals.org
January 2015 / Vol. 65 No. 1 • BioScience 59
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
magnitude of impact, provided that there
are good historical data to determine
when the invasion began (c1 in figure 3).
Of particular interest are comparisons
of sites before and after invasion (c2 in
­figure 3). This is only feasible under certain circumstances, such as in locations in
which there have been long-term monitoring programs (Magurran et al. 2010)
or monitoring before an anticipated
invasion took place (Roy et al. 2012).
However, in such cases, the long-term
temporal dynamics of the impacts of
alien species are generally not sufficiently
understood to give recommendations on
the optimal time scale of impact studies
(Yelenik and D’Antonio 2013). Moreover,
time series studies might encounter the
same confounding problems as comparisons between invaded and uninvaded
sites, given that differences over time
might be caused by other (confounding)
stressors acting simultaneously during an
Figure 2. Empirical approaches for forecasting impacts of alien species, starting invasion ­(figure 1, appendix S1).
If direct observations on the tempowith the most desirable data. If an alien species has a sufficiently documented
ral
dynamics of impacts are not feasible,
impact history in its invaded range, the patterns within the data could be
changes
in communities or ecosystem
analyzed statistically (e.g., using multivariate techniques or meta-analysis)
processes
might not be attributable to the
to construct quantitative or qualitative models of its impact (e.g., Ricciardi
presence
and
activity of the alien species
2003, Kulhanek et al. 2011). In cases in which no impact history is available,
but,
rather,
to
concurrent or preceding
the invasion history of the species could be used to predict its abundance—a
changes
in
the
environment
(e.g., grazing,
proxy for its level of impact—by relating variation in local abundance to
eutrophication,
changes
in
climate conlimiting physicochemical variables (e.g., Jokela and Ricciardi 2008). Otherwise,
ditions).
Whether
alien
species
are paspredictive information might be obtained from the impact (invasion) history of
sengers
or
drivers
of
change
is
difficult
to
functionally similar species or from trait-based models of high-impact invaders
resolve
by
observation
alone
(MacDougall
(e.g., Pyšek et al. 2012, Kumschick et al. 2013). Further information on the
suggested parameters appears in appendix S1. Source: Adapted with permission and Turkington 2005). For example, the
observed decline of native ladybird beetle
from Ricciardi (2003).
species in arboreal habitats in the UK
after invasion by the alien ladybird beetle
observed outcome can be confounded with between-site
Harmonia axyridis is also correlated with changes in maximum
differences not related to the introduced species. With this
temperature and rainfall among years (Brown et al. 2011).
in mind, such studies should select plots that are as closely
However, path analysis and structural equation modeling can
matched as possible for other abiotic and biotic features
sometimes be applied to disentangle the relative importance of
(Hejda et al. 2009). One approach is to correlate the magnialien species and other stressors to native species declines (e.g.,
tude of one or more impacts along a gradient of alien species
Light and Marchetti 2007, Hermoso et al. 2011).
abundance (b in figure 3). For instance, herbivore effects on
Although, in any aspect of ecology, the manipulation of
plant fitness are often density dependent, such that their
parameters is the best way to demonstrate causality, field
per capita effect is correlated with density (e.g., Trumble
removal experiments to identify the impacts of alien speet al. 1993). However, the relationship between per capita
cies (d in figure 3, appendix S2) have been reported in only
impact and alien species abundance remains to be examined
a small number of studies. The most prominent examples
for a range of taxa, systems, and environmental conditions.
concern the removal of alien plants, but field manipulaUnfortunately, it is often very difficult to find contemtion experiments represent less than 14% of the studies on
poraneous similar but uninvaded reference sites to contrast
the impacts of alien plants (Vilà et al. 2011). Comparing
with invaded sites. Under such circumstances, it would be
invaded plots with those from which alien species have been
preferable to study genuine chronosequences that enable an
removed offers a straightforward method to demonstrate
analysis of the relationships in the time since invasion and the
that ecological differences between these plots are linked
Overview Articles
60 BioScience • January 2015 / Vol. 65 No. 1
http://bioscience.oxfordjournals.org
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
Removal experiments for mobile
organisms are difficult to achieve in
practice, and the results from such
experiments are highly context dependent. There have now been many
eradications of alien animal species
worldwide (e.g., Pluess et al. 2012),
with sometimes counterintuitive results
on the dynamics of their prey (Rayner
et al. 2007). Furthermore, compared
with that of sessile species, the impact of
mobile species with large home ranges
(e.g., vertebrates) might be spatially
diluted and difficult to quantify at the
local scale. Eradications can be used
for comparisons of invaded communities before and after the removal of
the alien (e.g., Monks et al. 2014), but
other approaches, such as comparisons
Figure 3. Empirical approaches for studying the impacts of invasive alien species with other invaded and uninvaded sites,
might also be possible. For mobile speusing manipulated and unmanipulated plots: (a) Observational approach
cies with large home ranges, the use of
comparing invaded and uninvaded (reference) plots. (b) Observational
well-designed enclosures or fences to
approach along a gradient of alien species abundance (higher abundance is
compare large invaded and uninvaded
represented here by darker shading). (c1) Chronosequence of invasion (stages
areas might be one of the most realistic
of different time since invasion shown as discontinuous squares). (c2) A
options (Burns et al. 2012).
special case of the previous approach: a before- and after-invasion approach
The removal of an alien species does
comparing only two stages over time. (d) Experimental approach comparing
invaded and removal plots. (e) Experimental approach comparing removal and not necessarily (or not immediately) lead
to the restoration of preinvasion condiuninvaded reference plots. (f) Experimental approach comparing plots from
which the alien or the native species has been removed; these can be undertaken tions, particularly for some ecosystem
engineers that may have a legacy effect
to account for the disturbance effect in the removal experiments (comparing
on habitat conditions (Magnoli et al.
panels (f), (e), and (d)) or to test whether functionally similar native and alien
2013). It is therefore crucial to comspecies have different effects.
pare removal plots with uninvaded and
unmanipulated reference plots (e in figure 3). From a resto the effects of alien species. However, the outcomes of
toration perspective, a successful removal strategy would
these experiments can be confounded with disturbance
be one in which the ecosystem recovers along a trajectory
effects due to species removal. Disturbance can be minileading to a state similar to that in a reference site, not only
mized in various ways. For example, if the alien species is
in terms of species richness but also in terms of species coman annual plant, the invader can be removed at the seedling
position and ecosystem functioning. For example, following
stage (Hulme and Bremner 2006). Disturbance is, however,
the removal of monkey flowers (Mimulus guttatus) from a
often unavoidable if the invader is a perennial plant speriparian system, the resident plant community recovered
cies. Consequently, removal plots are often set in an earlier
and increased in species richness over time but toward a
successional stage than are intact invaded plots; even if
different community composition than that of uninvaded
they harbor high levels of species richness, their species
sites (Truscott et al. 2008). This demonstrates that different
composition can be different, and they are therefore not
methodological approaches can lead to different conclusions
exactly comparable, because many species regenerating in
based on extant impacts.
the removal plots are early colonizers that can, themselves,
In some cases, removals of alien species could be combe alien species (Truscott et al. 2008, Andreu et al. 2010).
pared with removals of closely related natives. For example,
In such cases, it is advantageous to combine the experifield removal experiments that have been conducted in the
mental removal of alien species with the removal of native
Bahamas to exclude the alien red lionfish (Pterois volitans)
species, where that is deemed appropriate (f in figure 3),
and test how the impact of this species compares with that of
to distinguish the alien–native effect from the disturbance
the coney grouper (Cephalopholis fulva, a native predator of
effect. For sessile species, comparing ecological differsimilar size and diet) showed that the alien species reduced
ences between areas in which aliens and natives have been
the abundance and richness of small coral-reef fishes more
removed will elucidate whether the effect of the alien is due
than of the native predator (Albins 2013). More studies
to species origin per se.
Overview Articles
Conclusions
Not only is research on the impacts of alien species necessary to understand why some species are more disruptive
than others and why some systems are more susceptible
to being disturbed by alien species, but it is also of practical importance in determining how limited management
resources should be allocated. The better our understanding
of impacts, the better equipped we will be to implement
effective management. Systematically gathering and synthesizing solid evidence of the impacts caused by alien species
facilitates communication with the public and better informs
policy- and decisionmakers. Disputes within the scientific
community about the role of alien species increases the perception of them being innocuous or equally likely to have
positive effects (but see Richardson and Ricciardi 2013). In
fact, many alien species cause substantial and sometimes
irreversible impacts, but we have not yet achieved a predictive understanding of when or where these impacts will
occur or which species will cause them.
http://bioscience.oxfordjournals.org
Furthermore, our synthesis points out that different
experimental methodologies are appropriate for different
taxa because of particular properties of the species and ecosystems involved, even though most methods are theoretically applicable for most organismal groups (appendix S2).
It is known, however, that using different methodological
approaches can lead to different conclusions (e.g., Truscott
et al. 2008). Moreover, sessile organisms are more frequently
studied than are mobile ones, which can potentially introduce bias. Further studies are required to determine the
extent to which such issues influence our evaluation and
knowledge of impacts and the perceived differences between
organismal groups.
A more balanced view of impacts and a standardized protocol of how to quantify impacts—that is, which parameters
to measure and which metrics to apply at invaded sites—are
needed. Therefore, we have proposed a set of parameters on
which to base the objective quantification of impacts. The
collation of information on these parameters will contribute
to a better understanding of context dependence and to a
robust framework for prioritization.
Acknowledgements
This article is a joint effort of the working group sImpact
that formed at a workshop supported by sDiv, the Synthesis
Centre for Biodiversity Sciences within the German Centre
for Integrative Biodiversity Research (iDiv) Halle–Jena–
Leipzig, funded by the German Research Foundation
(DFG; through grant no. FZT 118). We acknowledge support from the Swiss National Science Foundation and
the Drakenstein Trust (to SK); the Spanish Ministry of
Economy and Competitiveness and the Severo Ochoa
Programme for Centres of Excellence (Projects ConsoliderIngenio MONTES no. CSD2008-00040, no. RIXFUTUR
CGL2009-7515, and no. FLORMAS CGL2012-33801 to
MV); the COST Action TD1209 Alien Challenge (to MV,
FE, JMJ, PP, JP, SB, TMB, PEH, and WR); the Austrian
Climate Research Program (project no. K10AC1K00061
­“RAG-Clim” to FE); the ERA-Net BiodivERsA (project FFII),
with national funding from the DFG (grant no. JE 288/7-1
to JMJ); the Academy of Sciences of the Czech Republic
(grant no. RVO 67985939), the Czech Science Foundation
(grant no. 14-36079G Centre of Excellence PLADIAS, and
P504/11/1028 to PP and JP), and the Ministry of Education,
Youth and Sports of the Czech Republic (to PP and AM);
the Praemium Academiae award from the Academy of
Sciences of the Czech Republic (to PP); the Canadian
Aquatic Invasive Species Network and NSERC Canada (to
AR); the UK Natural Environment Research Council and
the Leverhulme Trust (to JTAD); the Department of Science
and Technology and National Research Foundation’s
Centre of Excellence for Invasion Biology (to SK and DMR)
and the National Research Foundation (grant no. 85417
to DMR); Charles University in Prague (project no. SVV
267204 to AM); and the German Academic Exchange
Service DAAD (to AS).
January 2015 / Vol. 65 No. 1 • BioScience 61
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
of this kind are needed to discern whether alien species
impacts represent the average effect or a magnified effect of
a single species in the community when it is dominant (f in
figure 3). However, such native-removal studies are only feasible and sensible if no negative conservation implications of
removing those natives are expected.
Manipulative species-addition field experiments are technically feasible (appendix S2; Meffin et al. 2010) but highly
challenging, because the prevention of the establishment and
spread of the alien species outside experimental plots has
to be a priority in the experimental setting. This is difficult
to achieve and might jeopardize the value of an experiment
intended to obtain observations of an interaction between
the additional alien species individuals and the recipient
community. An alternative is to perform species-addition
experiments in restricted conditions mimicking field conditions as much as possible. Mesocosms have mainly been used
to test the impacts of soil organisms and aquatic alien species
(appendix S2). Such studies can be informative regarding
particular impact mechanisms for species interactions but
are problematic for inferring impacts at the community and
ecosystem levels. Moreover, mesocosm and common-garden
experiments are usually too short term or restricted in scale
to predict long-term field conditions.
There are multiple ways to assess alien species impacts,
but no single method appears to have a clear advantage. We
advocate a four-way plot experimental design (uninvaded,
invaded, removal of natives, removal of aliens; a, d, e, and f in
figure 3), not only to reveal ecological impacts and to detect
regime shifts but also to determine the potential success of
restoration efforts. The use of large-scale removal programs
as a source of experimental data can be highly valuable if
they are carried out in such a way as to allow this recommended design. Spatial and temporal variation in impacts
must also be taken into account by careful replication and
monitoring of the sampled sites (Kueffer et al. 2013).
Overview Articles
Supplemental material
The supplemental material is available online at http://bioscience.oxfordjournals.org/lookup/suppl/doi:10.1093/biosci/
biu193/-/DC1.
References cited
62 BioScience • January 2015 / Vol. 65 No. 1
http://bioscience.oxfordjournals.org
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
Albins MA. 2013. Effects of invasive Pacific red lionfish Pterois volitans
versus a native predator on Bahamian coral-reef fish communities.
Biological Invasions 15: 29−43.
Andreu J, Manzano E, Dana ED, Bartomeus I, Vilà M. 2010. Vegetation
response after removal of the invader Carpobrotus spp. in coastal dunes.
Ecological Restoration 28: 440–448.
Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ. 2004. Avian
extinction risk and mammalian introductions on oceanic islands.
Science 305: 1955–1958.
Blackburn TM et al. 2014. Towards a unified classification of alien species
based on the magnitude of their environmental impacts. PLOS Biology
12 (art. e1001850).
Bomford M. 2008. Risk Assessment Models for Establishment of Exotic
Vertebrates in Australia and New Zealand. Invasive Animals Cooperative
Research Centre.
Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE. 2011.
Decline in native ladybirds in response to the arrival of Harmonia
axyridis (Coleoptera: Coccinellidae): Early evidence from England.
Ecological Entomology 36: 231–240.
Burns B, Innes J, Day T. 2012. The use and potential of pest-proof fencing for
ecosystem restoration and fauna conservation in New Zealand. Pages
65–90 in Somers MJ, Hayward MW, eds. Fencing for Conservation:
Restriction of Evolutionary Potential or a Riposte to Threatening
Processes? Springer.
Catford JA, Vesk P, Richardson DM, Pyšek P. 2012. Quantifying levels of
biological invasion: Towards the objective classification of invaded and
invasible ecosystems. Global Change Biology 18: 44–62.
D’Antonio CM, Vitousek PM. 1992. Biological invasions by exotic grasses,
the grass/fire cycle, and global change. Annual Review of Ecology and
Systematics 23: 63–87.
Dick JTA, et al. 2014. Advancing impact prediction and hypothesis testing
in invasion ecology using a comparative functional response approach.
Biological Invasions 16: 735–753.
Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM. 2007. The
interactive effects of habitat loss and species invasion on native species
decline. Trends in Ecology and Evolution 22: 489–496.
Dostál P, Müllerová J, Pyšek P, Pergl J, Klinerová T. 2013. The impact of an
invasive plant changes over time. Ecology Letters 16: 1277–1284.
Drenovsky RE, Grewell BJ, D’Antonio CM, Funk JL, James JJ, Molinari N,
Parker IM, Richards CL. 2012. A functional trait perspective in plant
invasion. Annals of Botany 110: 141–153.
Evans T, Kumschick S, Dyer E, Blackburn TM. 2014. Comparing determinants of alien bird impacts across two continents: implications
for risk assessment and management. Ecology and Evolution 4:
2957–2967.
Gaertner M, Den Breeÿen A, Hui C, Richardson DM. 2009. Impacts of alien
plant invasions on species richness in Mediterranean-type ecosystems: a
meta-analysis. Progress in Physical Geography 33: 319–338.
Gaertner M, Biggs R, te Beest M, Hui C, Molofsky J, Richardson DM. 2014.
Invasive plants as drivers of regime shifts: Identifying high priority
invaders that alter feedback relationships. Diversity and Distributions
20: 733–744.
Hejda M, Pyšek P, Jarošík V. 2009. Impact of invasive plants on the species
richness, diversity and composition of invaded communities. Journal of
Ecology 97: 393–403.
Hermoso V, Clavero M, Blanco-Garrido F, Prenda J. 2011. Invasive species
and habitat degradation in Iberian streams: an analysis of their role in
freshwater fish diversity loss. Ecological Applications 21: 175–188.
Hulme PE. 2006. Beyond control: Wider implications for the management
of biological invasions. Journal of Applied Ecology 43: 835–847.
Hulme PE, Bremner ET. 2006. Assessing the impact of Impatiens glandulifera on riparian habitats: Partitioning diversity components following
species removal. Journal of Applied Ecology 43: 43–50.
Hulme PE, Pyšek P, Jarošík V, Pergl J, Schaffner U, Vilà M. 2013. Bias and
error in understanding plant invasion impacts. Trends in Ecology and
Evolution 28: 212–218.
Jeschke JM, et al. 2014. Defining the impact of non-native species.
Conservation Biology 28: 1188–1194.
Jokela A, Ricciardi A. 2008. Predicting zebra mussel fouling on native mussels from physico-chemical variables. Freshwater Biology 53: 1845–1856.
Kestrup Å, Ricciardi A. 2009. Environmental heterogeneity limits the local
dominance of an invasive freshwater crustacean. Biological Invasions
11: 2095–2105.
Kueffer C, Pyšek P, Richardson DM. 2013. Integrative invasion science:
Model systems, multi-site studies, focused meta-analysis and invasion
syndromes. New Phytologist 200: 615–633.
Kulhanek SA, Ricciardi A, Leung B. 2011. Is invasion history a useful tool
for predicting the impacts of the world’s worst aquatic invasive species?
Ecological Applications 21: 189–202.
Kumschick S, Richardson DM. 2013. Species-based risk assessments for biological invasions: Advances and challenges. Diversity and Distributions
19: 1095–1105.
Kumschick S, Bacher S, Dawson W, Heikkilä J, Sendek A, Pluess T, Robinson
TB, Kühn I. 2012. A conceptual framework for prioritization of invasive
alien species for management according to their impact. NeoBiota 15:
69–100.
Kumschick S, Bacher S, Blackburn TM. 2013. What determines the impact of
alien birds and mammals in Europe? Biological Invasions 15: 785–797.
Leung B, et al. 2012. TEASIng apart alien species risk assessments: A framework for best practices. Ecology Letters 15: 1475–1493.
Light T, Marchetti MP. 2007. Distinguishing between invasions and habitat
changes as drivers of diversity loss among California’s freshwater fishes.
Conservation Biology 21: 434–446.
Linder HP, Bykova O, Dyke J, Etienne RS, Hickler T, Kühn I, Marion G,
Ohlemüller R, Schymanski SJ, Singer A. 2012. Biotic modifiers, environmental modulation and species distribution models. Journal of
Biogeography 39: 2179–2190.
Lodge DM. 1993. Biological invasions: Lessons for ecology. Trends in
Ecology and Evolution 8: 133–137.
MacDougall AS, Turkington R. 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42–55.
Mack MC, D’Antonio CM. 1998. Impacts of biological invasions on disturbance regimes. Trends in Ecology and Evolution 13: 195–198.
Magnoli SM, Kleinhesselink AR, Cushman JH. 2013. Responses to invasion
and invader removal differ between native and exotic plant groups in a
coastal dune. Oecologia 173: 1521–1530.
Magurran AE, Baillie SR, Buckland ST, Dick J McP, Elston DA, Scott EM,
Smith RI, Somerfield PJ, Watt AD. 2010. Long-term datasets in biodiversity research and monitoring: Assessing change in ecological communities through time. Trends in Ecology and Evolution 25: 574–582.
Meffin R, Miller AL, Hulme PE, Duncan RP. 2010. Experimental introduction of the alien weed Hieracium lepidulum reveals no significant
impact on montane plant communities in New Zealand. Diversity and
Distributions 16: 804–815.
Monks JM, Monks A, Towns DR. 2014. Correlated recovery of five lizard
populations following eradication of invasive mammals. Biological
Invasions 16: 167–175.
Nentwig W, Kühnel E, Bacher S. 2010. A generic impact-scoring system
applied to alien mammals in Europe. Conservation Biology 24: 302–311.
Parker IM et al. 1999. Impact: Toward a framework for understanding the
ecological effects of invaders. Biological Invasions 1: 3–19.
Pluess T, Cannon R, Jarošík V, Pergl J, Pyšek P, Bacher S. 2012. When are
eradication campaigns successful? A test of common assumptions.
Biological Invasions 14: 1365–1378.
Powell KI, Chase JM, Knight TM. 2011. A synthesis of plant invasion effects
on biodiversity across spatial scales. American Journal of Botany 98:
539–548.
Overview Articles
http://bioscience.oxfordjournals.org
meta-analysis of their effects on species, communities and ecosystems.
Ecology Letters 14: 702–708.
Vitousek PM. 1990. Biological invasions and ecosystem processes: Towards
an integration of population biology and ecosystem studies. Oikos 57:
7–13.
Yelenik SG, D’Antonio CM. 2013. Self-reinforcing impacts of plant invasions change over time. Nature 503: 517–520.
Sabrina Kumschick, Mirijam Gaertner, and David M. Richardson are affiliated with the Centre for Invasion Biology, in the Department of Botany and
Zoology at Stellenbosch University, in Matieland, South Africa. Montserrat
Vilà is affiliated with the Estación Biológica de Doñana, in Seville, Spain. Franz
Essl is affiliated with the Department of Conservation Biology, Vegetation and
Landscape Ecology at the University of Vienna, Austria. Jonathan M. Jeschke
is affiliated with Technische Universität München’s Department of Ecology
and Ecosystem Management, Restoration Ecology, in Freising-Weihenstephan,
Germany. Petr Pyšek and Agata Mrugała are affiliated with the Department
of Ecology, in the Faculty of Science of Charles University in Prague, and
PP and Jan Pergl are affiliated with the Department of Invasion Ecology,
in the Institute of Botany at the Academy of Sciences of the Czech Republic,
in Průhonice. Anthony Ricciardi is affiliated with the Redpath Museum,
at McGill University, in Montreal, Quebec, Canada. Sven Bacher is affiliated with the Department of Biology, in the Unit Ecology and Evolution at
the University of Fribourg, in Fribourg, Switzerland. Tim M. Blackburn is
affiliated with the Institute of Zoology of the Zoological Society of London,
United Kingdom, and with the Environment Institute, in the School of Earth
and Environmental Sciences, at the University of Adelaide, South Australia,
Australia. Jaimie T.A. Dick is affiliated with the Institute for Global Food
Security, in the School of Biological Sciences at Queen’s University Belfast,
Northern Ireland, United Kingdom. Thomas Evans is affiliated with Imperial
College London’s Silwood Park Campus, in Berkshire, United Kingdom.
Philip E. Hulme is affiliated with the Bio-Protection Research Centre, at
Lincoln University, in Christchurch, New Zealand. Ingolf Kühn and Agnieszka
Sendek are affiliated with the Helmholtz Centre for Environmental Research’s
Department of Community Ecology and with Martin-Luther-University
Halle–Wittenberg’s Institute of Biology/Geobotany and Botanical Garden, in
Halle, Germany, and IK and Marten Winter are affiliated with the German
Centre for Integrative Biodiversity Research Halle–Jena–Leipzig, in Leipzig,
Germany. Wolfgang Rabitsch is affiliated with Environment Agency Austria’s
Department of Biodiversity and Nature Conservation, in Vienna, Austria.
January 2015 / Vol. 65 No. 1 • BioScience 63
Downloaded from http://bioscience.oxfordjournals.org/ at Univerzita Karlova v Praze on December 29, 2014
Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M. 2012.
A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading
species’ traits and environment. Global Change Biology 18: 1725–1737.
Rayner MJ, Hauber ME, Imber MJ, Stamp RK, Clout MN. 2007. Spatial
heterogeneity of mesopredator release within an oceanic island.
Proceedings of the National Academy of Sciences of the USA 104:
20862–20865.
Ricciardi A. 2003. Predicting the impacts of an introduced species from its
invasion history: An empirical approach applied to zebra mussel invasions. Freshwater Biology 48: 972–981.
———. 2007. Are modern biological invasions an unprecedented form of
global change? Conservation Biology 21: 329–336.
Ricciardi A, Atkinson SK. 2004. Distinctiveness magnifies the impact of
biological invaders in aquatic ecosystems. Ecology Letters 7: 781–784.
Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL. 2013. Progress toward
understanding the ecological impacts of nonnative species. Ecological
Monographs 83: 263–282.
Richardson DM, Ricciardi A. 2013. Misleading criticisms of invasion science: A field guide. Diversity and Distributions 19: 1461–1467.
Roy HE, et al. 2012. Invasive alien predator causes rapid declines of native
European ladybirds. Diversity and Distributions 18: 717–725.
Scheffer M, et al. 2012. Anticipating critical transitions. Science 338:
344–348.
Strauss SY, Webb CO, Salamin N. 2006. Exotic taxa less related to native
species are more invasive. Proceedings of the National Academy of
Sciences of the USA 103: 5841–5845.
Strayer DL, Eviner VT, Jeschke JM, Pace ML. 2006. Understanding the long-term
effects of species invasions. Trends in Ecology and Evolution 21: 645–651.
Trumble JT, Kolodny-Hirsch DM, Ting IP. 1993. Plant compensation for
arthropod herbivory. Annual Review of Entomology 38: 93–119.
Truscott AM, Palmer SCF, Soulsby C, Westaway S, Hulme PE. 2008.
Consequences of invasion by the alien plant Mimulus guttatus on the
species composition and soil properties of riparian plant communities
in Scotland. Perspectives in Plant Ecology, Evolution and Systematics
10: 231–240.
Vilà M, et al. 2010. How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment.
Frontiers in Ecology and the Environment 8: 135–144.
Vilà M, Espinar J, Hejda M, Hulme P, Jarošík V, Maron J, Pergl J, Schaffner
U, Sun Y, Pyšek P. 2011. Ecological impacts of invasive alien plants: A